Abstract
The purpose of this systematic review was to provide updated evidence synthesis of the effectiveness of exercise training in patients with obesity undergoing bariatric surgery to improve cardio-metabolic risk. We systematically searched the MEDLINE, EMBASE, Scopus, Cochrane, and Web of Science databases. The studies selected were those in which an exercise-based intervention was performed after bariatric surgery, a control group was present, and at least one of the following outcomes was investigated: VO2max or VO2peak, resting heart rate (RHR), blood pressure, lipid profile, glucose, and insulin. The study quality was assessed using the PEDro scale and the data were meta-analyzed with a random effects model, comparing control groups to intervention groups using standardized measurements. Twenty articles were included in the systematic review and fourteen (70%) in the meta-analysis. Significant differences were observed between the control and intervention groups (always in favor of exercise) for absolute VO2max / VO2peak (ES = 0.317; 95% CI = 0.065, 0.569; p = 0.014), VO2max / peak relative to body weight (ES = 0.673; 95% CI = 0.287, 1.060; p = 0.001), HDL cholesterol (ES = 0.22; 95% CI = 0.009, 0.430; p = 0.041) and RHR (ES = -0.438; 95% CI = -0.753, -0.022; p = 0.007). No effects were observed for either systolic or diastolic blood pressure. Exercise training for patients undergoing bariatric surgery appears to be effective in improving absolute and relative VO2max / VO2peak, HDL cholesterol and reducing the RHR. More intervention studies using (better) exercise interventions are needed before discarding their effects on other cardiometabolic risk factors. This systematic review and meta-analysis has been registered in Prospero (CRD42020153398).
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Data exchange is not applicable since no databases were generated during the present study.
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Comprehensive Meta Analysis V2.0.
References
Obesity and overweight. World Heal. Organ. 2018. Available from: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight
Koliaki C, Liatis S, Kokkinos A. Obesity and cardiovascular disease: revisiting an old relationship. Metabolism. Elsevier Inc.; 2019;92:98–107. Available from: https://doi.org/10.1016/j.metabol.2018.10.011
Apovian CM. Obesity : Definition, Comorbidities, Causes, and Burden. Am J Manag Care. 2016;22:176–85.
Soriano-Maldonado A, Aparicio VA, Félix-Redondo FJ, Fernández-Bergés D. Severity of obesity and cardiometabolic risk factors in adults: Sex differences and role of physical activity. The HERMEX study. Int J Cardiol. Elsevier Ireland Ltd; 2016;223:352–9.
Ricci C, Gaeta M, Rausa E, Macchitella Y, Bonavina L. Early impact of bariatric surgery on type II diabetes, hypertension, and hyperlipidemia: a systematic review, meta-analysis and meta-regression on 6,587 patients. Obes Surg. 2014;24:522–8.
Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292:1724–37.
Lascaris B, Pouwels S, Houthuizen P, Dekker LR, Nienhuijs SW, Bouwman RA, et al. Cardiac structure and function before and after bariatric surgery: a clinical overview. Clin Obes. 2018;8:434–43.
Cuspidi C, Rescaldani M, Tadic M, Sala C, Grassi G. Effects of bariatric surgery on cardiac structure and function: A systematic review and meta-analysis. Am J Hypertens. 2014;27:146–56.
Ortega F, Vilallonga R, Xifra G, Sabater M, Ricart W, Fernández-Real J. Bariatric surgery acutely changes the expression of inflammatory and lipogenic genes in obese adipose tissue. Surg Obes Relat Dis. 2016;12:357–62.
Coen PM, Carnero EA, Goodpaster BH. Exercise and Bariatric Surgery: An Effective Therapeutic Strategy. Exerc Sport Sci Rev United States. 2018;46:262–70.
Bellicha A, Ciangura C, Portero P, J.M.O. Effectiveness of exercise training after bariatric surgery - a systematic literature review and meta-analysis. Obes Rev. 2018;19:1544–56.
Soriano-Maldonado A, Villa-González E, Ferrer-Márquez M, Artero EG. Replicability of exercise programs following bariatric surgery. Atherosclerosis. A. Soriano-Maldonado, Department of Education, Faculty of Education Sciences, University of Almería, Carretera de Sacramento, s/n, La Cañada, Almería, Spain; 2018;278:330–1.
Lin X, Zhang X, Guo J, Roberts CK, McKenzie S, Wu WC, et al. Effects of exercise training on cardiorespiratory fitness and biomarkers of cardiometabolic health: A systematic review and meta-analysis of randomized controlled trials. J Am Heart Assoc. 2015;4:e002014.
Kohl HW. Physical activity and cardiovascular disease: Evidence for a dose response. Med Sci Sports Exerc. 2001;33.
Haennel RG, Lemire F. Physical activity to prevent cardiovascular disease. How much is enough? Can Fam Physician. 2002;48:65–71.
Lanza IR. Enhancing the metabolic benefits of bariatric surgery: Tipping the scales with exercise. Diabetes. 2015;64:3656–8.
Carretero-Ruiz A, Olvera-Porcel MC, Cavero-Redondo I, Álvarez-Bueno C, Martínez-Vizcaíno V, Ferrer-Márquez M, et al. Effects of Exercise Training on Weight Loss in Patients Who Have Undergone Bariatric Surgery: a Systematic Review and Meta-Analysis of Controlled Trials. Obes Surg. 2019;29.
Moher D, Liberati A, Tetzlaff J, Altman DG, Prisma Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264–9.
Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions. Cochrane. 2011.
Verhagen A, De Vet H, De Bie RA, Kessels AGH, Boers M, Bouter LM, et al. The Delphi list: A criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J Clin Epidemiol. 1998;51:1235–41.
Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro Scale for Rating Quality of Randomized Controlled Trials. Phys Ther. 2003;83:713–21.
Sun S, Pan W, Wang LL. A Comprehensive Review of Effect Size Reporting and Interpreting Practices in Academic Journals in Education and Psychology. J Educ Psychol. 2010;102:989–1004.
Hedges LV, Olkin I. Statistical methods for meta-analysis. San Diego: Academic Press; 1985.
Dersimonian R, Laird N. Meta-Analysis in Clinical Trials*. Control Clin Trials. 1986;7:177–88.
Higgins JPT, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343.
Cochran WG. The combination of estimates from different experiments. Biometrics Biometrics. 1954;10:101–29.
Irwig L, Macaskill P, Berry G, Glasziou P. Bias in meta-analysis detected by a simple, graphical test. Graphical test is itself biased BMJ. 1998;316:1–11.
Sterne JAC, Gavaghan D, Egger M. Publication and related bias in meta-analysis: Power of statistical tests and prevalence in the literature. J Clin Epidemiol. 2000;53:1119–29.
Tardif I, Auclair A, Piché ME, Biertho L, Marceau S, Hould FS, et al. Impact of a 12-Week Randomized Exercise Training Program on Lipid Profile in Severely Obese Patients Following Bariatric Surgery. Obes Surg Obesity Surgery. 2020;30:3030–6.
Auclair A, Harvey J, Leclerc J, Piché ME, O’Connor K, Nadreau É, et al. Determinants of Cardiorespiratory Fitness After Bariatric Surgery: Insights From a Randomised Controlled Trial of a Supervised Training Program. Can J Cardiol. 2020;
Coen PM, Tanner CJ, Helbling NL, Dubis GS, Hames KC, Xie H, et al. Clinical trial demonstrates exercise following bariatric surgery improves insulin sensitivity. J Clin Invest. American Society for Clinical Investigation; 2015;125:248–57.
Coen PM, Menshikova E V., Distefano G, Zheng D, Tanner CJ, Standley RA, et al. Exercise and weight loss improve muscle mitochondrial respiration, lipid partitioning, and insulin sensitivity after gastric bypass surgery. Diabetes. B.H. Goodpaster, Translational Research Institute for Metabolism and Diabetes, Florida Hospital, Orlando, FL, United States; 2015;64:3737–50.
Mundbjerg LH, Stolberg CR, Cecere S, Bladbjerg E-M, Funch-Jensen P, Gram B, et al. Supervised Physical Training Improves Weight Loss After Roux-en-Y Gastric Bypass Surgery: A Randomized Controlled Trial. Obesity. 2018;26:828–37.
Mundbjerg LH, Stolberg CR, Bladbjerg EM, Funch-Jensen P, Juhl CB, Gram B. Effects of 6 months supervised physical training on muscle strength and aerobic capacity in patients undergoing Roux-en-Y gastric bypass surgery: a randomized controlled trial. Clin Obes. 2018;8:227–35.
Nunez Lopez YO, Coen PM, Goodpaster BH, Seyhan AA. Gastric bypass surgery with exercise alters plasma microRNAs that predict improvements in cardiometabolic risk. Int J Obes Nature Publishing Group. 2017;41:1121–30.
Stolberg CR, Mundbjerg LH, Funch-Jensen P, Gram B, Juhl CB, Bladbjerg E-M. Effects of gastric bypass followed by a randomized study of physical training on markers of coagulation activation, fibrin clot properties, and fibrinolysis. Surg Obes Relat Dis. 2018;14:918–26.
Woodlief TL, Carnero EA, Standley RA, Distefano G, Anthony SJ, Dubis GS, et al. Dose response of exercise training following roux-en-Y gastric bypass surgery: A randomized trial. Obesity. 2015;23:2454–61.
Gil S, Peçanha T, Dantas WS, Murai IH, Merege-Filho CAA, de Sá-Pinto AL, et al. Exercise Enhances the Effect of Bariatric Surgery in Markers of Cardiac Autonomic Function. Obes Surg. 2020;
Dantas WS, Roschel H, Murai IH, Gil S, Davuluri G, Axelrod CL, et al. Exercise-induced increases in insulin sensitivity after bariatric surgery are mediated by muscle extracellular matrix remodeling. Diabetes. 2020;69:1675–91.
Castello V, Simoes RP, Bassi D, Catai AM, Arena R, Borghi-Silva A. Impact of aerobic exercise training on heart rate variability and functional capacity in obese women after gastric bypass surgery. Obes Surg United States. 2011;21:1739–49.
Castello-Simões V, Polaquini Simões R, Beltrame T, Bassi D, Maria Catai A, Arena R, et al. Effects of aerobic exercise training on variability and heart rate kinetic during submaximal exercise after gastric bypass surgery – a randomized controlled trial. Disabil Rehabil. 2013;35:334–42.
Herring LY, Stevinson C, Carter P, Biddle JH, Bowrey D, Sutton C, et al. The effects of supervised exercise training 12–24 months after bariatric surgery on physical function and body composition: A randomised controlled trial. Int J Obes. 2017;41:909–16.
Huck C. Effects of supervised resistance training on fitness and functional strength in patients succeeding bariatric surgery. J Strength Cond Res. 2015;29:589–95.
Onofre T, Carlos R, Oliver N, Felismino A, Fialho D, Corte R, et al. Effects of a Physical Activity Program on Cardiorespiratory Fitness and Pulmonary Function in Obese Women after Bariatric Surgery: a Pilot Study. Obes Surg. 2017;27:2026–33.
Stegen S, Derave W, Calders P, Van Laethem C, Pattyn P. Physical fitness in morbidly obese patients: Effect of gastric bypass surgery and exercise training. Obes Surg. 2011;21:61–70.
Shah M, Snell PG, Rao S, Adams-Huet B, Quittner C, Livingston EH, et al. High-volume exercise program in obese bariatric surgery patients: A randomized, controlled trial. Obesity. 2011;19:1826–34.
Marc-Hernández A, Ruiz-Tovar J, Aracil A, Guillén S, Moya-Ramón M. Effects of a High-Intensity Exercise Program on Weight Regain and Cardio-metabolic Profile after 3 Years of Bariatric Surgery: A Randomized Trial. Sci Rep. Nature Research; 2020;10.
Marchesi F, De Sario G, Reggiani V, Tartamella F, Giammaresi A, Cecchini S, et al. Road Running After Gastric Bypass for Morbid Obesity: Rationale and Results of a New Protocol. Obes Surg. 2015;25:1162–70.
Coen PM, Tanner CJ, Helbling NL, Dubis GS, Hames KC, Xie H, et al. Clinical trial demonstrates exercise following bariatric surgery improves insulin sensitivity. J Clin Invest. B.H. Goodpaster, Translational Research Institute for Metabolism and Diabetes, Florida Hospital - Sanford-Burnham Medical Research Institute, 301 East Princeton Street, Orlando, FL, United States; 2015;125:248–57.
da Silva ALG, Sardeli AV, André LD, Severin R, de Oliveira CR, Hassan C, et al. Exercise Training Does Improve Cardiorespiratory Fitness in Post-Bariatric Surgery Patients. Obes Surg. 2019;29:1416–9.
Kim J, Park HY, Lim K. Effects of 12 weeks of combined exercise on heart rate variability and dynamic pulmonary function in obese and elderly Korean women. Iran J Public Health. 2018;47:74–81.
Vogelsang TW, Hanel B, Kristoffersen US, Petersen CL, Mehlsen J, Holmquist N, et al. Effect of eight weeks of endurance exercise training on right and left ventricular volume and mass in untrained obese subjects: A longitudinal MRI study. Scand J Med Sci Sport. 2008;18:354–9.
Cocks M, Shaw CS, Shepherd SO, Fisher JP, Ranasinghe A, Barker TA, et al. Sprint interval and moderate-intensity continuous training have equal benefits on aerobic capacity, insulin sensitivity, muscle capillarisation and endothelial eNOS/NAD(P)Hoxidase protein ratio in obese men. J Physiol. 2016;594:2307–21.
Carretero-Ruiz A, del Carmen Olvera-Porcel M, Cavero-Redondo I, Álvarez-Bueno C, Martínez-Vizcaíno V, Ferrer-Márquez M, et al. Correction to: Effects of Exercise Training on Weight Loss in Patients Who Have Undergone Bariatric Surgery: a Systematic Review and Meta-Analysis of Controlled Trials. Obes Surg. 2019;29.
Williams MA, Haskell WL, Ades PA, Amsterdam EA, Bittner V, Franklin BA, et al. Resistance exercise in individuals with and without cardiovascular disease: 2007 update: A scientific statement from the American Heart Association Council on Clinical Cardiology and Council on Nutrition, Physical Activity, and Metabolism. Circulation. 2007;116:572–84.
Greene NP, Martin SE, Crouse SF. Acute exercise and training alter blood lipid and lipoprotein profiles differently in overweight and obese men and women. Obesity. 2012;20:1618–27.
Kodama S, Tanaka S, Saito K, Shu M, Sone Y, Onitake F, et al. Effect of aerobic exercise training on serum levels of high-density lipoprotein cholesterol: A meta-analysis. Arch Intern Med. 2007;167:999–1008.
Sarzynski MA, Ruiz-ramie JJ, Barber JL, Slentz CA, John W, Mcgarrah RW, et al. The effects of increasing exercise intensity and dose on multiple measures of high-density lipoprotein function. Arter Thromb Vasc Biol. 2018;38:943–52.
Woudberg NJ, Mendham AE, Katz AA, Goedecke JH, Lecour S. Exercise intervention alters HDL subclass distribution and function in obese women. Lipids Health Dis. Lipids in Health and Disease; 2018;17:232.
Trajkovska KT, Topuzovska S. High-density lipoprotein metabolism and reverse cholesterol transport: Strategies for raising HDL cholesterol. Anatol J Cardiol. 2017;18:149–54.
Kontush A, Lindahl M, Lhomme M, Calabresi L, Chapman MJ. Davidson WS. Structure of HDL: Particle subclasses and molecular components. High Density Lipoproteins; 2015. p. 3–51.
Daniel JR, Alan RT. The not-so-simple HDL story: A new era for quantifying HDL and cardiovascular risk? Nat. Med: Nature Publishing Group; 2012.
Dantas WS, Gil S, Murai IH, Costa-Hong V, Peçanha T, Merege-Filho CAA, et al. Reversal of Improved Endothelial Function After Bariatric Surgery Is Mitigated by Exercise Training. J Am Coll Cardiol. American College of Cardiology Foundation; 2018;72:2278–9.
Villa-González E, Barranco-Ruiz Y, Rodríguez-Pérez MA, Carretero-Ruiz A, García-Martínez JM, Hernández-Martínez A, et al. Supervised exercise following bariatric surgery in morbid obese adults: CERT-based exercise study protocol of the EFIBAR randomised controlled trial. BMC Surg. 2019;19:127. Available from: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85071761586&doi=10.1186%2Fs12893-019-0566-9&partnerID=40&md5=07921fd9a65663d95ee43fafc9575b9a
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This work was funded by the Spanish Ministry of Economy and Competitiveness (MINECO), Plan Nacional de I + D + i call RETOS 2016 (grant number DEP2016‐74926‐R) and the Spanish Ministry of Science, Innovation and Universities, Plan Nacional de I + D + i call RETOS 2018 (grant number RTI2018-093302-A-I00). EM-R was supported by the Spanish Ministry of Science, Innovation and Universities (FPU18/01107).
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ACR, IC-R, CA-B and EGA designed the review and meta-analysis. ACR and EMR conducted the review and carried out the meta-analysis. ACR wrote the article with the support of EGA, VM-V, MF-M, and AS-M, while EGA provided clinical and epidemiological support. EGA was the principal investigator and guarantor. All authors reviewed and approved the final version of the manuscript.
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Carretero-Ruiz, A., Martínez-Rosales, E., Cavero-Redondo, I. et al. Impact of exercise training after bariatric surgery on cardiometabolic risk factors: a systematic review and meta-analysis of controlled trials. Rev Endocr Metab Disord 22, 891–912 (2021). https://doi.org/10.1007/s11154-021-09651-3
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DOI: https://doi.org/10.1007/s11154-021-09651-3